Things we never knew: maggots are covered with eyes!

I work with maggots. Not big fat maggots you use for fishing, but Drosophila maggots. They are incredibly simple, but are capable of performing most of the behaviours shown by the adult fly (with the obvious exceptions of mating and flying). The tiny flyDrosophila was chosen by Thomas Hunt Morgan at the beginning of the last century when he decided to study evolution. After a few years, his attempt to make Drosophilaevolve was coming to nothing, when he found a white-eyed mutant fly. The rest, as they say, is history, as Morgan and his students revealed the laws of genetics that had been sketched out half a century earlier by Mendel.

Throughout the 20th century, Drosophila was studied by geneticists, and it was the first multicellular organism to have its genome sequenced, just as the new millenium dawned. Now there are hundreds of laboratories around the world studying the genetics and neurobiology of Drosophila. It would be fair enough to imagine that we knew almost everything there is to know about which cells do what in the fly, and even more so in its juvenile, more simple form, the maggot. How wrong that would be!

An article soon to be published by Nature from the world-famous laboratory of Lily and Yuh Jan describes the astonishing finding that Drosophila maggots – and, you can be pretty sure, virtually every other kind of fly maggot – is covered with tiny “eyes”. Nobody had any idea that this was the case.

Up until today, the maggot’s “eyes” were thought to be a group of 12 cells called Bolwig’s organ. They are named after the Danish scientist Niels Bolwig, who did his doctoral thesis on vision in fly maggots, and later went on to pioneer studies of primates in the wild; he died in 2004. There are two Bolwig’s organs, which you might imagine are the dome-shaped things on the front of the maggot’s face below. These structures are in fact the maggot’s “nose” or dorsal organ (my favourite bit of a maggot).

This proves that there must be some other cells in the maggot that can detect light (there was no change in temperature when the maggots had a light shone on them). Furthermore, Bolwig-less maggots did not respond to green or red light, but did avoid short-wavelength light at high intensities.

The paper reports that a particular set of cells in the maggot’s body wall, called class IV dendritic arborization neurons, responded to light – even when they were grown, isolated, in culture. These cells cover the whole of the maggot, as seen in this dramatic image – all the green cells are class IV neurons, and every one is an “eye”!

Amazingly, it turns out that these cells also express a taste receptor, Gr28b, which may be directly involved in sensing light, although this has yet to be demonstrated. This isn’t quite so surprising in that in the nematode worm C. elegans, a similar gene is also involved in responses to light. Another protein, TrpA1, which is involved in responses to light in the adult fly, is necessary for these class IV neurons to respond.

The authors conclude:

Our study has uncovered unexpected light-sensing machinery, which could be critical for foraging larvae to avoid harmful sunlight, desiccation and predation. By providing precedence for photoreceptors strategically placed away from the eyes, our finding of an array of class IV dendritic arborization neurons with elaborate dendrites tiling the entire body wall, and acting as light-sensing antennae, raises the question of whether other animals with eyes might also possess extra-ocular photoreceptors for more thorough light detection and behavioural response.

Even more importantly, this surprising result shows quite how much we have yet to discover about this animal about which, many people might have thought, we knew virtually everything. We know so much, but so little!

Is there any indication that the whole-body vision is directional? That is, if you shine a light on just half of the maggot, will it move towards the dark end?

If so…it seems to make more sense to state that the maggot is a single eye, rather than that it is covered in them.

Imagine what it would be like if all your melanin-producing cells were replaced with comparable photoreceptors (and the requisite neural mechanisms to wire it into your brain plus proper brain circuitry to make sense of it). On the one hand, there wouldn’t be any optical focusing mechanism. On the other hand, the image would be of fantastically high resolution, enough that the brain would almost certainly be capable of producing an extremely detailed all-encompassing three-dimensional map of your surroundings. Add a couple primitive freckle-sized higher-density eyepits randomly here and there…the result would be a visual system of staggering ability.

It’s not hard to imagine a larva-like visual system arising early in an evolutionary system instead of the more familiar eye. If we ever make contact with another intelligence (the chances of which are negligible), they may well be from such a system….

The lack of focusing mechanisms is actually a big problem, since there wouldn’t be any images as such on your skin. Without a lens to focus the light from your surroundings, you’d just perceive the average light intensity.

Even more importantly, this surprising result shows quite how much we have yet to discover about this animal about which, many people might have thought, we knew virtually everything. We know so much, but so little!

Indeed. I had just been expounding on this week’s Nature’s focus on glia. We construct stories, but must never forget that there are threads of which we remain unaware.

Furthermore, Bolwig-less maggots did not respond to green or red light, but did avoid short-wavelength light at high intensities.

Has anyone compared the wavelength (or “color temperature,” familiar to photographers) of the light that maggots avoid to the wavelength of light put out by the sun, both full-on direct sunlight and other conditions, such as “open shade” on a bright day, etc?

“color temperature” is associated with human vision and does not necessarily apply to another animal. For example, some mammals do not filter out UV so they perceive light differently. Some mammals do not have color receptors.

I was wondering though how intense the lights were – is there any response at all to green light or red light, for example if we use a 1mW green or red laser? What is the light detection mechanism and why is it only sensitive to the shorter wavelengths? Other materials in nature behave that way and many of the early experiments on the photoelectric effect were of that nature.

With white light from a Xenon lamp (approximating sunlight’s), the Bolwig-less animals responded similarly to wild-type animals to an intensity of 0.57mW per square millimeter (a bit less than a sunny day in San Francisco).
The Bolwig’s organ was required for avoiding weaker light (down to 0.088mW/mm2 in white light).

I wouldn’t call them ‘eyes’ though – merely photoreceptors (such as the cones and rods in a mammal’s eyes). For me an eye would have to have a lens of sorts. Of course there is a possibility of a photoreceptor and lens combination which results in a directional or an extra-sensitive light detector but does not produce images.

[…] by some band called Drosophila Excrementus, but this is actually a nifty science post. I just read this article from Jerry Coyne (who’s book, Why Evolution Is True, is utterly fantastic and you should read […]